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Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex

Abstract

The primary visual cortex of primates and carnivores is organized into columns of neurons with similar preferences for stimulus orientation, but the developmental origin and function of this organization are still matters of debate. We found that the orientation preference of a cortical column is closely related to the population receptive field of its ON and OFF thalamic inputs. The receptive field scatter from the thalamic inputs was more limited than previously thought and matched the average receptive field size of neurons at the input layers of cortex. Moreover, the thalamic population receptive field (calculated as ON – OFF average) had separate ON and OFF subregions, similar to cortical neurons in layer 4, and provided an accurate prediction of the preferred orientation of the column. These results support developmental models of orientation maps that are based on the receptive field arrangement of ON and OFF visual inputs to cortex.

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Figure 1: Geniculate afferents making monosynaptic connections with a cortical orientation column were identified by STCSD.
Figure 2: The ON – OFF population receptive field of the geniculate inputs predicts the preferred orientation of the cortical column.
Figure 3: The ON – OFF population receptive field from connected geniculate inputs provides the most accurate prediction of cortical orientation preference.
Figure 4: The orientation prediction from the ON – OFF population receptive field of geniculate inputs is highly significant and accurate, as demonstrated by Monte Carlo simulations.
Figure 5: The probability that two geniculate cells will make monosynaptic connections with the same orientation column is exponentially related to the distance between the geniculate receptive fields.
Figure 6: The ratio of ON/OFF afferents within each orientation column was correlated with the ratio of ON/OFF afferent strength, estimated by STCSD.

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Acknowledgements

We thank C. Weng for helping with some experiments. This work was supported by the US National Institutes of Health (grants EY05253 to J.M.A. and MH085357 to H.A.S.).

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J.J., Y.W. and J.M.A. performed the experiments, J.J., Y.W., J.M.A. and H.A.S. were involved in data analysis, and J.M.A., H.A.S., J.J. and Y.W. wrote the paper.

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Correspondence to Jose M Alonso.

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Jin, J., Wang, Y., Swadlow, H. et al. Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex. Nat Neurosci 14, 232–238 (2011). https://doi.org/10.1038/nn.2729

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